P-Element Mutations Affecting Embryonic Peripheral Nervous System Development in Drosophila melanogaster

INVESTIGATIONS

P-Element Mutations Affecting Embryonic Peripheral Nervous System Development in Drosophila melanogaster

A. Kania, A. Salzberg, M. Bhat, D. D'Evelyn, Y. He, I. Kiss and H. J. Bellen
Howard Hughes Medical Institute, Department of Molecular and Human Genetics, Division of Neuroscience, Department of Cell Biology, Baylor College of Medicine, Houston, Texas 77030

The Drosophila embryonic peripheral nervous system (PNS) is an excellent model system to study the molecular mechanisms governing neural development. To identify genes controlling PNS development, we screened 2000 lethal P-element insertion strains. The PNS of mutant embryos was examined using the neural specific marker MAb 22C10, and 92 mutant strains were retained for further analysis. Genetic and cytological analysis of these strains shows that 42 mutations affect previously isolated genes that are known to be required for PNS development: longitudinals lacking (19), mastermind (15), numb (4), big brain (2), and spitz (2). The remaining 50 mutations were classified into 29 complementation groups and the P-element insertions were cytologically mapped. The mutants were classified in five major classes on the basis of their phenotype: gain of neurons, loss of neurons, organizational defects, pathfinding defects and morphological defects. Herein we report the preliminary phenotypic characterization of each of these complementation groups as well as the embryonic lacZ expression pattern of each P-element strain. Our analysis indicates that in most of the P-element insertion strains, the lacZ reporter gene is not expressed in the developing PNS.

This article has been cited by other articles:

X. Wu, M. Yamada-Mabuchi, E. J. Morris, P. S. Tanwar, L. Dobens, S. Gluderer, S. Khan, J. Cao, H. Stocker, E. Hafen, et al.
The Drosophila homolog of human tumor suppressor TSC-22 promotes cellular growth, proliferation, and survival
PNAS, April 8, 2008; 105(14): 5414 - 5419.
[Abstract] [Full Text] [PDF]

J. Chen, X. Shi, R. Padmanabhan, Q. Wang, Z. Wu, S. C. Stevenson, M. Hild, D. Garza, and H. Li
Identification of novel modulators of mitochondrial function by a genome-wide RNAi screen in Drosophila melanogaster
Genome Res., January 1, 2008; 18(1): 123 - 136.
[Abstract] [Full Text] [PDF]

E. N. Mindorff, D. D. O'Keefe, A. Labbe, J. P. Yang, Y. Ou, S. Yoshikawa, and D. J. van Meyel
A Gain-of-Function Screen for Genes That Influence Axon Guidance Identifies the NF-{kappa}B Protein Dorsal and Reveals a Requirement for the Kinase Pelle in Drosophila Photoreceptor Axon Targeting
Genetics, August 1, 2007; 176(4): 2247 - 2263.
[Abstract] [Full Text] [PDF]

B. Dermaut, K. K. Norga, A. Kania, P. Verstreken, H. Pan, Y. Zhou, P. Callaerts, and H. J. Bellen
Aberrant lysosomal carbohydrate storage accompanies endocytic defects and neurodegeneration in Drosophila benchwarmer
J. Cell Biol., July 4, 2005; 170(1): 127 - 139.
[Abstract] [Full Text] [PDF]

L. M. Escudero, E. Caminero, K. L. Schulze, H. J. Bellen, and J. Modolell
Charlatan, a Zn-finger transcription factor, establishes a novel level of regulation of the proneural achaete/scute genes of Drosophila
Development, March 15, 2005; 132(6): 1211 - 1222.
[Abstract] [Full Text] [PDF]

A. Inbal, D. Levanon, and A. Salzberg
Multiple roles for u-turn/ventral veinless in the development of Drosophila PNS
Development, June 1, 2003; 130(11): 2467 - 2478.
[Abstract] [Full Text] [PDF]

C. L. Dilda and T. F. C. Mackay
The Genetic Architecture of Drosophila Sensory Bristle Number
Genetics, December 1, 2002; 162(4): 1655 - 1674.
[Abstract] [Full Text] [PDF]

C. Robin, R. F. Lyman, A. D. Long, C. H. Langley, and T. F. C. Mackay
hairy: A Quantitative Trait Locus for Drosophila Sensory Bristle Number
Genetics, September 1, 2002; 162(1): 155 - 164.
[Abstract] [Full Text] [PDF]

S. E. Mohr and W. M. Gelbart
Using the P{wHy} Hybrid Transposable Element to Disrupt Genes in Region 54D-55B in Drosophila melanogaster
Genetics, September 1, 2002; 162(1): 165 - 176.
[Abstract] [Full Text] [PDF]

T. E. Rusten, R. Cantera, F. C. Kafatos, and R. Barrio
The role of TGF{beta} signaling in the formation of the dorsal nervous system is conserved between Drosophila and chordates
Development, August 1, 2002; 129(15): 3575 - 3584.
[Abstract] [Full Text] [PDF]

H. Schenkel, S. Hanke, C. De Lorenzo, R. Schmitt, and B. M. Mechler
P Elements Inserted in the Vicinity of or Within the Drosophila snRNP SmD3 Gene Nested in the First Intron of the Ornithine Decarboxylase Antizyme Gene Affect Only the Expression of SmD3
Genetics, June 1, 2002; 161(2): 763 - 772.
[Abstract] [Full Text] [PDF]

H. A. Dworak, M. A. Charles, L. B. Pellerano, and H. Sink
Characterization of Drosophila hibris, a gene related to human nephrin
Development, November 1, 2001; 128(21): 4265 - 4276.
[Abstract] [Full Text] [PDF]

K. W. Dobie, C. D. Kennedy, V. M. Velasco, T. L. McGrath, J. Weko, R. W. Patterson, and G. H. Karpen
Identification of Chromosome Inheritance Modifiers in Drosophila melanogaster
Genetics, April 1, 2001; 157(4): 1623 - 1637.
[Abstract] [Full Text]

V Orgogozo, F Schweisguth, and Y Bellaiche
Lineage, cell polarity and inscuteable function in the peripheral nervous system of the Drosophila embryo
Development, January 3, 2001; 128(5): 631 - 643.
[Abstract] [PDF]

S. N. Prokopenko, Y. He, Y. Lu, and H. J. Bellen
Mutations Affecting the Development of the Peripheral Nervous System in Drosophila: A Molecular Screen for Novel Proteins
Genetics, December 1, 2000; 156(4): 1691 - 1715.
[Abstract] [Full Text]

B. Nait–Oumesmar, A. B. Copperman, and R. A. Lazzarini
Placental Expression and Chromosomal Localization of the Human Gcm 1 Gene
J. Histochem. Cytochem., July 1, 2000; 48(7): 915 - 922.
[Abstract] [Full Text]

S. Abdelilah-Seyfried, Y.-M. Chan, C. Zeng, N. J. Justice, S. Younger-Shepherd, L. E. Sharp, S. Barbel, S. A. Meadows, L. Y. Jan, and Y. N. Jan
A Gain-of-Function Screen for Genes That Affect the Development of the Drosophila Adult External Sensory Organ
Genetics, June 1, 2000; 155(2): 733 - 752.
[Abstract] [Full Text]

N Ben-Arie, B. Hassan, N. Bermingham, D. Malicki, D Armstrong, M Matzuk, H. Bellen, and H. Zoghbi
Functional conservation of atonal and Math1 in the CNS and PNS
Development, January 3, 2000; 127(5): 1039 - 1048.
[Abstract] [PDF]

L. Dobens, J. Peterson, J Treisman, and L. Raftery
Drosophila bunched integrates opposing DPP and EGF signals to set the operculum boundary
Development, January 2, 2000; 127(4): 745 - 754.
[Abstract] [PDF]

A. C. Spradling, D. Stern, A. Beaton, E. J. Rhem, T. Laverty, N. Mozden, S. Misra, and G. M. Rubin
The Berkeley Drosophila Genome Project Gene Disruption Project: Single P-Element Insertions Mutating 25% of Vital Drosophila Genes
Genetics, September 1, 1999; 153(1): 135 - 177.
[Abstract] [Full Text]

C. Byars, K. Bates, and A Letsou
The dorsal-open group gene raw is required for restricted DJNK signaling during closure
Development, January 11, 1999; 126(21): 4913 - 4923.
[Abstract] [PDF]

A. Holmes and J. Heilig
Fasciclin II and Beaten path modulate intercellular adhesion in Drosophila larval visual organ development
Development, January 1, 1999; 126(2): 261 - 272.
[Abstract] [PDF]

B. A. Hassan, S. N. Prokopenko, S. Breuer, B. Zhang, A. Paululat, and H. J. Bellen
skittles, a Drosophila Phosphatidylinositol 4-Phosphate 5-Kinase, Is Required for Cell Viability, Germline Development and Bristle Morphology, But Not for Neurotransmitter Release
Genetics, December 1, 1998; 150(4): 1527 - 1537.
[Abstract] [Full Text]

I. P. Ivanov, K. Simin, A. Letsou, J. F. Atkins, and R. F. Gesteland
The Drosophila Gene for Antizyme Requires Ribosomal Frameshifting for Expression and Contains an Intronic Gene for snRNP Sm D3 on the Opposite Strand
Mol. Cell. Biol., March 1, 1998; 18(3): 1553 - 1561.
[Abstract] [Full Text]

E Kurant, C. Pai, R Sharf, N Halachmi, Y. Sun, and A Salzberg
Dorsotonals/homothorax, the Drosophila homologue of meis1, interacts with extradenticle in patterning of the embryonic PNS
Development, January 3, 1998; 125(6): 1037 - 1048.
[Abstract] [PDF]

W. Chia, R. Kraut, P. Li, X. Yang, and M. Zavortink
On the Roles of inscuteable in Asymmetric Cell Divisions in Drosophila
Cold Spring Harb Symp Quant Biol, January 1, 1997; 62(0): 79 - 87.
[Abstract] [PDF]

Y. Akiyama, T. Hosoya, A. M. Poole, and Y. Hotta
The gcm-motif: A novel DNA-binding motif conserved in Drosophila and mammals
PNAS, December 10, 1996; 93(25): 14912 - 14916.
[Abstract] [Full Text] [PDF]

C Merli, D E Bergstrom, J A Cygan, and R K Blackman
Promoter specificity mediates the independent regulation of neighboring genes.
Genes & Dev., May 15, 1996; 10(10): 1260 - 1270.
[Abstract] [PDF]

				J. Chen, X. Shi, R. Padmanabhan, Q. Wang, Z. Wu, S. C. Stevenson, M. Hild, D. Garza, and H. Li Identification of novel modulators of mitochondrial function by a genome-wide RNAi screen in Drosophila melanogaster Genome Res., January 1, 2008; 18(1): 123 - 136. [Abstract] [Full Text] [PDF]

				E. N. Mindorff, D. D. O'Keefe, A. Labbe, J. P. Yang, Y. Ou, S. Yoshikawa, and D. J. van Meyel A Gain-of-Function Screen for Genes That Influence Axon Guidance Identifies the NF-{kappa}B Protein Dorsal and Reveals a Requirement for the Kinase Pelle in Drosophila Photoreceptor Axon Targeting Genetics, August 1, 2007; 176(4): 2247 - 2263. [Abstract] [Full Text] [PDF]

				B. Dermaut, K. K. Norga, A. Kania, P. Verstreken, H. Pan, Y. Zhou, P. Callaerts, and H. J. Bellen Aberrant lysosomal carbohydrate storage accompanies endocytic defects and neurodegeneration in Drosophila benchwarmer J. Cell Biol., July 4, 2005; 170(1): 127 - 139. [Abstract] [Full Text] [PDF]

				L. M. Escudero, E. Caminero, K. L. Schulze, H. J. Bellen, and J. Modolell Charlatan, a Zn-finger transcription factor, establishes a novel level of regulation of the proneural achaete/scute genes of Drosophila Development, March 15, 2005; 132(6): 1211 - 1222. [Abstract] [Full Text] [PDF]

				A. Inbal, D. Levanon, and A. Salzberg Multiple roles for u-turn/ventral veinless in the development of Drosophila PNS Development, June 1, 2003; 130(11): 2467 - 2478. [Abstract] [Full Text] [PDF]

				C. L. Dilda and T. F. C. Mackay The Genetic Architecture of Drosophila Sensory Bristle Number Genetics, December 1, 2002; 162(4): 1655 - 1674. [Abstract] [Full Text] [PDF]

				C. Robin, R. F. Lyman, A. D. Long, C. H. Langley, and T. F. C. Mackay hairy: A Quantitative Trait Locus for Drosophila Sensory Bristle Number Genetics, September 1, 2002; 162(1): 155 - 164. [Abstract] [Full Text] [PDF]

				S. E. Mohr and W. M. Gelbart Using the P{wHy} Hybrid Transposable Element to Disrupt Genes in Region 54D-55B in Drosophila melanogaster Genetics, September 1, 2002; 162(1): 165 - 176. [Abstract] [Full Text] [PDF]

				T. E. Rusten, R. Cantera, F. C. Kafatos, and R. Barrio The role of TGF{beta} signaling in the formation of the dorsal nervous system is conserved between Drosophila and chordates Development, August 1, 2002; 129(15): 3575 - 3584. [Abstract] [Full Text] [PDF]

				H. Schenkel, S. Hanke, C. De Lorenzo, R. Schmitt, and B. M. Mechler P Elements Inserted in the Vicinity of or Within the Drosophila snRNP SmD3 Gene Nested in the First Intron of the Ornithine Decarboxylase Antizyme Gene Affect Only the Expression of SmD3 Genetics, June 1, 2002; 161(2): 763 - 772. [Abstract] [Full Text] [PDF]

				H. A. Dworak, M. A. Charles, L. B. Pellerano, and H. Sink Characterization of Drosophila hibris, a gene related to human nephrin Development, November 1, 2001; 128(21): 4265 - 4276. [Abstract] [Full Text] [PDF]

				K. W. Dobie, C. D. Kennedy, V. M. Velasco, T. L. McGrath, J. Weko, R. W. Patterson, and G. H. Karpen Identification of Chromosome Inheritance Modifiers in Drosophila melanogaster Genetics, April 1, 2001; 157(4): 1623 - 1637. [Abstract] [Full Text]

				V Orgogozo, F Schweisguth, and Y Bellaiche Lineage, cell polarity and inscuteable function in the peripheral nervous system of the Drosophila embryo Development, January 3, 2001; 128(5): 631 - 643. [Abstract] [PDF]

				S. N. Prokopenko, Y. He, Y. Lu, and H. J. Bellen Mutations Affecting the Development of the Peripheral Nervous System in Drosophila: A Molecular Screen for Novel Proteins Genetics, December 1, 2000; 156(4): 1691 - 1715. [Abstract] [Full Text]

				B. Nait–Oumesmar, A. B. Copperman, and R. A. Lazzarini Placental Expression and Chromosomal Localization of the Human Gcm 1 Gene J. Histochem. Cytochem., July 1, 2000; 48(7): 915 - 922. [Abstract] [Full Text]

				S. Abdelilah-Seyfried, Y.-M. Chan, C. Zeng, N. J. Justice, S. Younger-Shepherd, L. E. Sharp, S. Barbel, S. A. Meadows, L. Y. Jan, and Y. N. Jan A Gain-of-Function Screen for Genes That Affect the Development of the Drosophila Adult External Sensory Organ Genetics, June 1, 2000; 155(2): 733 - 752. [Abstract] [Full Text]

				N Ben-Arie, B. Hassan, N. Bermingham, D. Malicki, D Armstrong, M Matzuk, H. Bellen, and H. Zoghbi Functional conservation of atonal and Math1 in the CNS and PNS Development, January 3, 2000; 127(5): 1039 - 1048. [Abstract] [PDF]

				L. Dobens, J. Peterson, J Treisman, and L. Raftery Drosophila bunched integrates opposing DPP and EGF signals to set the operculum boundary Development, January 2, 2000; 127(4): 745 - 754. [Abstract] [PDF]

				A. C. Spradling, D. Stern, A. Beaton, E. J. Rhem, T. Laverty, N. Mozden, S. Misra, and G. M. Rubin The Berkeley Drosophila Genome Project Gene Disruption Project: Single P-Element Insertions Mutating 25% of Vital Drosophila Genes Genetics, September 1, 1999; 153(1): 135 - 177. [Abstract] [Full Text]

				C. Byars, K. Bates, and A Letsou The dorsal-open group gene raw is required for restricted DJNK signaling during closure Development, January 11, 1999; 126(21): 4913 - 4923. [Abstract] [PDF]

				A. Holmes and J. Heilig Fasciclin II and Beaten path modulate intercellular adhesion in Drosophila larval visual organ development Development, January 1, 1999; 126(2): 261 - 272. [Abstract] [PDF]

				B. A. Hassan, S. N. Prokopenko, S. Breuer, B. Zhang, A. Paululat, and H. J. Bellen skittles, a Drosophila Phosphatidylinositol 4-Phosphate 5-Kinase, Is Required for Cell Viability, Germline Development and Bristle Morphology, But Not for Neurotransmitter Release Genetics, December 1, 1998; 150(4): 1527 - 1537. [Abstract] [Full Text]

				I. P. Ivanov, K. Simin, A. Letsou, J. F. Atkins, and R. F. Gesteland The Drosophila Gene for Antizyme Requires Ribosomal Frameshifting for Expression and Contains an Intronic Gene for snRNP Sm D3 on the Opposite Strand Mol. Cell. Biol., March 1, 1998; 18(3): 1553 - 1561. [Abstract] [Full Text]

				E Kurant, C. Pai, R Sharf, N Halachmi, Y. Sun, and A Salzberg Dorsotonals/homothorax, the Drosophila homologue of meis1, interacts with extradenticle in patterning of the embryonic PNS Development, January 3, 1998; 125(6): 1037 - 1048. [Abstract] [PDF]

				W. Chia, R. Kraut, P. Li, X. Yang, and M. Zavortink On the Roles of inscuteable in Asymmetric Cell Divisions in Drosophila Cold Spring Harb Symp Quant Biol, January 1, 1997; 62(0): 79 - 87. [Abstract] [PDF]

				Y. Akiyama, T. Hosoya, A. M. Poole, and Y. Hotta The gcm-motif: A novel DNA-binding motif conserved in Drosophila and mammals PNAS, December 10, 1996; 93(25): 14912 - 14916. [Abstract] [Full Text] [PDF]

				C Merli, D E Bergstrom, J A Cygan, and R K Blackman Promoter specificity mediates the independent regulation of neighboring genes. Genes & Dev., May 15, 1996; 10(10): 1260 - 1270. [Abstract] [PDF]